The impact of taphonomic data on phylogenetic resolution: Helenodora inopinata (Carboniferous, Mazon Creek Lagerstätte) and the onychophoran stem lineage

Murdock et al. BMC Evolutionary Biology (2016) 16:19 DOI 10.1186/s12862-016-0582-7 RESEARCH ARTICLE Open Access The impact of taphonomic data on phylogenetic resolution: Helenodora inopinata (Carboniferous, Mazon Creek Lagerstätte) and the onychophoran stem lineage Duncan J. E. Murdock, Sarah E. Gabbott and Mark A. Purnell* Abstract Background: The origin of the body plan of modern velvet worms (Onychophora) lies in the extinct lobopodians of the Palaeozoic. Helenodora inopinata, from the Mazon Creek Lagerstätte of Illinois (Francis Creek Shale, Carbondale Formation, Middle Pennsylvanian), has been proposed as an intermediate between the “weird wonders” of the Cambrian seas and modern terrestrial predatory onychophorans. The type material of H. inopinata, however, leaves much of the crucial anatomy unknown. Results: Here we present a redescription of this taxon based on more complete material, including new details of the head and posterior portion of the trunk, informed by the results of experimental decay of extant onychophorans. H. inopinata is indeed best resolved as a stem-onychophoran, but lacks several key features of modern velvet worms including, crucially, those that would suggest a terrestrial mode of life. Conclusions: The presence of H. inopinata in the Carboniferous demonstrates the survival of a Cambrian marine morphotype, and a likely post-Carboniferous origin of crown-Onychophora. Our analysis also demonstrates that taphonomically informed tests of character interpretations have the potential to improve phylogenetic resolution. Keywords: Panarthropoda, Lobopodia, Onychophora, Mazon Creek, Taphonomy Background Lobopodians are extinct worm-like animals characterised by their unsegmented lobopodous limbs. Known principally from Lower Palaeozoic Lagerstätten, some lobopodian taxa have been proposed to have affinities with extant Onychophora, but their precise relationships are unclear; recent analyses have recovered lobopodian taxa as stem-Euarthropoda, stem-Panarthropoda and stemOnychophora [1–4]. Correctly determining which clades particular lobopodian taxa are affiliated with has the potential to reveal important aspects of early panarthropod evolution. In the post-Palaeozoic fossil record, examples * Correspondence: Department of Geology, University of Leicester, University Road, Leicester LE1 7RH, UK of unequivocal terrestrial onychophorans are known from Cretaceous [5] and Eocene [6, 7] amber. Helenodora inopinata Thompson and Jones [8], from the Mazon Creek Lagerstätte of Illinois (Francis Creek Shale, Carbondale Formation, Middle Pennsylvanian), is claimed as the oldest terrestrial lobopodian [8] and is generally regarded as a stem-onychophoran more closely related to extant onychophorans than to Cambrian lobopodians [9]. Yet the evidence for this phylogenetic placement is scant, with considerable uncertainty caused by poor preservation of details of the head. Some new details of the anterior region of H. inopinata have recently been described by Haug et al. [10], alongside a description of a second Mazon Creek lobopodian, Carbotubulus waloszeki. The © 2016 Murdock et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Murdock et al. BMC Evolutionary Biology (2016) 16:19 discovery of additional specimens permits us to make a full redescription of H. inopinata, and to re-evaluate the interpretations of Thompson and Jones [8]. Furthermore, by incorporating the results of recent work on experimental decay of onychophorans into taphonomic analysis of character preservation we demonstrate that failure to include taphonomic evidence can lead to widespread loss of resolution in the results of phylogenetic analysis. Based on these new observations, in particular the absence of jaws, claws and slime papillae, we interpret H. inopinata as a stem-onychophoran and find no evidence for the proposed terrestrial mode of life. Results and discussion Systematic palaeontology Phylum ONYCHOPHORA Grube 1853 Genus HELENODORA Thompson and Jones 1980 Remarks Helenodora has been designated as a junior synonym of Ilyodes Scudder 1890 [11], but we consider this to be incorrect. Ilyodes was first described as belonging to the Myriapoda [12], and some 90 years later Helenodora inopinata was described as an onychophoran-like animal [8]. The similarity of these taxa and as yet undescribed material from Montceau-les-Mines [13, 14], led to the suggestion that they were synonymous [15]. Scudder [12] erected two species of Ilyodes: Ilyodes divisa and Ilyodes elongata. Re-examination of the type material clearly demonstrates significant differences between I. elongata, I. divisa and H. inopinata. Ilyodes elongata is a long (min. 161 mm) and thin (max. 4 mm) parallel-sided tube bearing a large number of segments (up to 166) and lacking clear limbs (Fig. 1a, b; Additional file 1). This lack of similarity demonstrates that I. elongata is not synonymous with H. inopinata. Helenodora inopinata and I. divisa are more directly comparable, sharing an annulated trunk with approximately the same number of annulae per limb-bearing segment (Fig. 1c, d; Additional file 1), but we argue that synonymising these taxa is incorrect for two reasons. First, that there are differences in the number of limbs: comparing similar length portions of the trunk, the holotype of I. divisa bears 15 limbs, and tapers in one direction, from a width of 5.5 to 3 mm, whereas, H. inopinata bears typically 20 limbs, is 6 mm wide at the widest point, and tapers in both directions. If we reconstruct I. divisa with a complete body of the same general proportions as H. inopinata, I. divisa would possess far more than the maximum of 20 walking limbs seen in any of the known material of H. inopinata. This evidence, that I. divisa bore a different number of limbs to H. inopinata, makes synonymy unlikely, but we cannot rule out the possibility. This brings us to the second, and more important reason not to synonymize: the Page 2 of 14 holotype of I. divisa preserves scant evidence of its original anatomy – little more than trunk annulations and limbs – and thus possesses too few taxonomically informative characters for it to be reliably differentiated from other fossil lobopodian taxa. Consequently, we deem Ilyodes divisa to be a nomen dubium. Of the options available to rectify this situation, selection of a neotype from among Scudder’s material is not possible as he included only (...truncated)